In 2020, 18 of these new fighter jets will land at the Vermont Air National Guard. Hard to believe but the Pentagon started working on a new fighter jet 17-years ago.
For supporters, the F-35 represents the future.
"This is going to be the fighter for most of the world, the Western World at least, for the next 30, 40 years," says Lieutenant Colonel Matt Renbarger, 58th Fighter Squadron Commander.
But it's the F-35s' past that concerns critics.
Headlines tell a story of years of delays, cost overruns, and problems with the jets. Right now, they still can't fly at night or during bad weather.
"That's how we have been fighting our wars is at night and all weather. To have that capability and start to train with that capability is critical to this program," says Colonel Todd Canterbury, 33rd Fighter Wing Commander.
Even the process of developing the F-35 helmet has been plagued with problems.
That was supposed to give pilots an advantage by seeing images from cameras around the plane. But the view was sometimes jittery.
"Is there a certain level of mistrust, I guess, of what some camera can do?" asked FOX44/ABC22's Matt Austin.
"Every pilot has a healthy level of mistrust of any airplane they're flying because if you trust it too much obviously it can get you into trouble," says Renbarger.
Renbarger is an F-35 pilot and commands the 58th Fighter Squadron at Florida's Eglin Air Force Base. He says his team is supposed to be finding problems.
"In a way, you're almost a guinea pig right now in this whole thing," asked Austin.
"We're okay with it because we're on the leading edge. We've all done this and everyone volunteered to come down here. And they knew the airplane was not going to be perfectly complete," says Renbarger.
Renbarger says the idea is testing and training on the jets will lead to improvements in the jets being produced in the future.
"The guys that are flying this aircraft 5,10, 15 years from now get a better F-35," says Renbarger.
Problems are being solved at Eglin.
Pilots as they were getting out of the jet were knocking a button off the throttle. So the crew that fixes the planes, the maintainers, designed a cover which costs $100. A lot less than the $6,000 solution by the plane's manufacturer.
Improvements are coming to the jets too.
Canterbury is in charge of training F-35 pilots and its crew. He says the planes should soon start flying at night or in bad weather.
"It's a software and hardware fix to the airplane they were working on. The software, these new airplanes that I have on the ramp, have the software involved," says Canterbury.
And he says the helmets have been improved too.
But even when the jets are ready for combat, it's inevitable many critics still won't be satisfied.
"They're noisy, they've cost so much money, they're so far behind. What do you say to them?" asked Austin.
"We talk to them about how we need to advance air power in the Air Force," says Renbarger.
"What do you think 5, 10, 20 years from now, people are going to say about the F-35?" asked Austin.
"I think it's going to be a huge success story," says Renbarger.
At least for now, the program has major concerns.
The Pentagon just released a new report updating the F-35 program.
It found the jets' computer system development is behind, the helmets are still having problems, and there are concerns about reliability and maintenance.
The report also cast doubts about the jets being ready for combat as soon as next year.
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